Epiphytic Macrolichens in Seoul: 35 Years After the First Lichen Study in Korea
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Research Paper J. Ecol. Field Biol. 34(4): 381-391, 2011 Journal of Ecology and Field Biology Epiphytic macrolichens in Seoul: 35 years after the first lichen study in Korea Chorong Ahn1,3, Eunmi Chang2 and Hyesoon Kang1,* 1School of Biological Science and Chemistry, Sungshin Women's University, Seoul 142-732, Korea 2Ziin Consulting Institute, Seoul 110-070, Korea 3Present Address: Department of Forest Conservation, Korea Forest Research Institute, Seoul 130-712, Korea Abstract Many lichens have been used as bioindicators for air pollutants such as SO2. The first ecological study on lichens in Korea was conducted in 1975 by Kim and Lee, disclosing that areas adjacent to the center of Seoul were lichen deserts. Air qual- ity in Seoul has improved significantly since the 1980s. However, the distribution of lichen species has not been reevalu- ated since then. We examined the spatial and temporal pattern of lichen distribution by selecting six (inner city green [ICG] and four (outer city green [OCG]) sites, based on the distance from the city center of Seoul and the land use pattern. The change in lichen distribution was related to yearly mean concentrations of SO2, NO2, and O3 for the years 1980-2009. Four and 13 lichen species were found in ICGs and OCGs, respectively. Although mean sample numbers per species were much higher in the former, species richness tended to increase with distance from the city center. Since 1980, SO2 has declined drastically to < 0.01 ppm in both ICGs and OCGs, indicating that SO2 is no longer a limiting factor for lichen establishment and growth. In contrast, NO2 has increased steadily for 20 years (1989-2009) and a considerable proportion of lichen species in both ICGs and OCGs are known as nitrophilic or pollution-tolerant species. Appearance of nitrophiles in both ICGs and OCGs and the dominance of a few lichen species in ICGs may reflect the effects of the increase in NO2. In contrast to SO2 and NO2, O3 was higher in OCGs, but it was difficult to identify a causal relationship between O3 and lichen distribution. Key words: air pollutants, bioindicator, lichens, Seoul, temporal and spatial variation INTRODUCTION Air pollutants clog urban cities; thus, it is difficult to and deciduous parts (Nash 2008). Therefore, epiphytic judge the quality of the atmosphere with just a few com- macrolichens have been used as air pollution bioindi- ponents. In this case, we can judge air quality by analyzing cators since lichen extinction was first observed in Paris the response of species to several air pollutants in con- (Nylander 1866, cited in Hawksworth and Rose 1970). sideration. In particular, epiphytic macrolichens on tree Until the mid-late 20th century, many studies revealed bark are excellent air pollution bioindicators. For exam- that a high concentration of SO2 disturbs the growth of li- ple, they receive nutrition and moisture through the thal- chens (Hawksworth and Rose 1970, Sugiyama et al. 1976, lus surface, and they have long lives. They also are able to Eversman 1978, McCune 1988, Nimis et al. 1990). Results concentrate pollutants, because they do not have cuticles of these studies also indicated that lichen loss was con- Open Access http://dx.doi.org/10.5141/JEFB.2011.040 Received 08 August 2011, Accepted 09 September 2011 This is an Open Access article distributed under the terms of the Creative *Corresponding Author Commons Attribution Non-Commercial License (http://creativecommons. org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, E-mail: [email protected] distribution, and reproduction in any medium, provided the original work Tel: +82-2-920-7475 is properly cited. pISSN: 1975-020X eISSN: 2093-4521 Copyright © The Ecological Society of Korea 381 http://jefb.org J. Ecol. Field Biol. 34(4): 381-391, 2011 spicuous near the city center or pollution sources. For ex- to air pollution sources (Hur and Kim 2000), and taxo- ample, 129 lichen species within 16 km of London became nomic diversity (Park 1990, Ka et al. 1997, Moon 1998). extinct between 1800 and 1970 (Laundon 1970). Con- However, the extent of lichen studies is very limited. Thus, versely, the number of lichen species tended to increase analyses have not been conducted on whether lichens with distance from the city center. In a study in London, have established themselves in inner city greens (ICGs), Rose and Hawksworth (1981) showed that areas in the and, if they have, what species have done so, what lichens 3 atmosphere with SO2 > 0.04 ppm (120-130 µg/m ) were exist outside the city, and what the species composition lichen deserts where lichen existence was impossible. and richness are in comparison to Kim and Lee (1975). Interestingly, lichens are recolonizing areas that used to The spatial and temporal patterns of lichen distribution be lichen deserts (Henderson-Sellers and Seaward 1979, are critical data to set standards for Seoul’s atmosphere Rose and Hawksworth 1981, Hawksworth and McManus policy and for an overall evaluation of nature conserva- 1989, Bates et al. 1990, Seaward 1997). tion policy. Although SO2 has decreased recently, nitrogen oxides In this study, we attempted to solve the following ques- (NOx) such as NO and NO2, and O3 have been increasing. tions: 1) In Seoul, do species composition and richness The change in air pollutants has been accompanied by a differ between inner and outer city greens (OCGs)?; 2) Are decrease in Lecanora conizaeoides in North America and there any changes in species composition and richness Europe, which is an SO2-tolerant species (Bates et al. 2001, since the initial study conducted 35 years ago?; 3) Are the Hauck et al. 2001), as well as an increase in pollution- particular lichens’ temporal and spatial distributions re- tolerant species such as Phaeophyscia orbicularis, Phys- lated to the level of SO2, NO2, or O3? cia adescendens, and Xanthoria parietina (Seaward 1997) and nitrophilic species such as Candelaria concolor and Phaeophyscia rubropulchra (Sigal and Nash 1983, de Bak- MATERIALS AND METHODS ker 1989, Jovan and McCune 2005). Furthermore, global warming acts as a new threat to symbiotic lichens (Geiser Study sites and sampling and Neitlich 2007). Reports of changes in lichen distribu- tion and air quality are occurring simultaneously in urban Seoul is located in the center of the Korean Peninsula and natural environments, suggesting that multi-disci- (126°59" E, 37°34" N) and is 30.30 km long and 36.78 km plinary approaches to lichens are necessary. across with a total area of 605.52 km2. The Han River flows According to the first ecological study on Korean li- through the center of the city, crossing in a west to east chens by Kim and Lee (1975), areas within 5 km of Gwang- direction. Namsan stands close to the center of the city. hwamun (city center hereafter) were lichen deserts. By Twenty-six mountains border the edge of the city (Seoul 1991, this area expanded to 15 km from the city center Metropolitan Government 2010). According to climate and coincided with areas that had an SO2 concentration data (30 year average from 1971-2000), Seoul’s mean tem- > 0.01 ppm (Kim 1991). Considering the phytotoxic ef- perature is 12.2°C, relative humidity is 66.8%, yearly rain- fects of SO2 on lichens, their results revealed that air qual- fall is 1,344 mm, and yearly mean wind speed is 2.4 m/s ity in Seoul was quite poor from 1970-1980. However, the (Korea Meteorological Administration 2001). Clean Air Act was enacted in 1990, leading to a decrease Lichen investigations were conducted in areas that in SO2 concentration in Seoul. Specifically, the concentra- matched the following three criteria: 1) green areas locat- tion has decreased after 1991 to < 0.04 ppm and has been ed 5, 10, 15, and 20 km from the city center; 2) areas that maintained < 0.01 ppm since 1998 (Ministry of Environ- were formed long enough ago for lichens to have become ment 2010). Assuming 0.04 ppm SO2 as a tolerance limit, it established; 3) areas where studies have been conducted would take approximately 5 years for an epiphytic lichen previously, so that temporal comparisons would be pos- on rocks such as Lecanora muralis to establish in an en- sible. Consequently, we selected the following ten sites, vironment (Henderson-Sellers and Seaward 1979). If so, six within and four outside a 10 km radius from the city the lichens that became extinct due to their SO2 sensitivity center (Fig. 1). Six ICGs (Boramae Park, Chandeokgung, could have become reestablished by now in Seoul. Dosan Park, Namsan Park, Samnung Park, and Sangdo In Korea, lichen studies have been conducted on the Park) were selected from parks and palaces with long distribution in relation to pollution centers (Lee et al. histories of greens located in areas with a relatively high 1993, 1994, Yu et al. 1995, Chu and Kim 1998, Kim and level of air pollution (Oh and Chung 2007). Four OCGs Kang 2001), selection of bioindicator species in response (Bukhansan, Cheonggyesan, Gwanaksan, and Suraksan) http://dx.doi.org/10.5141/JEFB.2011.040 382 Epiphytic macrolichens in Seoul had been changed. For example, Cladonia bacillaris was changed to C. macilenta. Lichen identification Specimens were identified based on exterior character- istics and a chemical composition analysis. We examined the thallus and reproductive structures and conducted chemical analyses following the color test (Nylander 1866), microcrystal tests (Asahina 1937), and thin layer chromatography (Culberson 1972). Data analysis Following LeBlanc and De Sloover (1970), we calculated the ecological index, Q, to reflect the number of species coexisting with a particular lichen species at each site: Fig.